A unique mating strategy without physical contact during fertilization in Bombay Night Frogs (Nyctibatrachus humayuni) with the description of a new form of amplexus and female call

Abstract

Anurans show the highest diversity in reproductive modes of all vertebrate taxa, with a variety of associated breeding behaviours. One striking feature of anuran reproduction is amplexus. During this process, in which the male clasps the female, both individuals’ cloacae are juxtaposed to ensure successful external fertilization. Several types of amplexus have evolved with the diversification of anurans, and secondary loss of amplexus has been reported in a few distantly related taxa. Within Nyctibatrachus, a genus endemic to the Western Ghats of India, normal axillary amplexus, a complete loss of amplexus, and intermediate forms of amplexus have all been suggested to occur, but many species remain unstudied. Here, we describe the reproductive behaviour of N. humayuni, including a new type of amplexus. The dorsal straddle, here defined as a loose form of contact in which the male sits on the dorsum of the female prior to oviposition but without clasping her, is previously unreported for anurans. When compared to known amplexus types, it most closely resembles the form of amplexus observed in Mantellinae. Furthermore, we prove that, opposed to the situation in most anurans, male semen release happens before egg deposition. We hypothesize that the male ejaculates on the female’s dorsum and that sperm subsequently runs from her back and hind legs before fertilizing the eggs. A second feature characterizing anuran breeding is the advertisement call, mostly produced solely by males. Despite recent descriptions of several new Nyctibatrachus species, few studies have explored their vocal repertoire. We describe both the male advertisement call and a female call for N. humayuni. The presence of a female call has not been reported within Nyctibatrachidae, and has been reported in less than 0.5% of anuran species. Altogether, our results highlight a striking diversity and several unique aspects of Nyctibatrachus breeding behaviour.

The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice

“…Species with derived mating behavior without amplexus often lack release calls (e.g., Malagasy frogs in the subfamily Mantellinae; ; but see Willaert et al 2016 for release calls in Nyctibatrachidae), but this subcategory is in general observed across the majority of anuran families. Release calls can differ among closely related species (e.g., Castellano et al 2002a) and have been proposed as a possible taxonomic character (Grenat & Martino 2013).…”

Much more than a clasp: Evolutionary pattern of amplexus diversity in anurans

“…Our study represents a unique large dataset on amplexus types for anurans, and allows to highlight three amplexus types (loose amplexus, gular amplexus, scapular amplexus) that have been overlooked in key literature references (i.e. Duellman & Trueb, 1986; Wells, 2007; Vitt & Caldwell, 2014; Pough et al ., 2016; Willaert et al, 2016). We hope that further studies about breeding behavior in anurans include detailed observations and descriptions that could reveal novelty aspects associated to diversity of breeding strategies in vertebrates, even in those lineages considered as well studied.…”

“…We defined the documented amplexus types (Fig. 1) following Duellman & Trueb (1986) and Willaert et al ., (2016), but also considering the following clarifications: First, in several species it has been reported that the amplexus type might change at the moment of oviposition (e.g. Anomaloglossus bebei and Brachycephalus ephippium ; Bourne et al, 2001, Pombal et al ., 1994; see supplementary material for more examples).…”

“…For Nyctibratrachus humayumi (Nyctibatrachidae), it was reported that this species lacks amplexus (Kunte, 2004), but it was later observed that N. humayumi has a dorsal straddle amplexus (Willaert et al, 2016). In another case, the authors cite a pectoral amplexus for Nasikabatrachus sahyadrensis (Sooglossidae) (Zachariah et al, 2012), but based on the detailed description by the authors, we consider this behavior to be a new type of amplexus.…”

Vocalisation and its association with androgens and corticosterone in a night frog (Nyctibatrachus humayuni) with unique breeding behaviour

“…The Bombay night frog, Nyctibatrachus humayuni (Family: Nyctibatrachidae), is one of the 35 species of night frogs described from India (Garg, Suyesh, Sukesan, & Biju, ). The frog is endemic to montane and submontane streams of the Western Ghats and exhibits unique courtship and breeding behaviour (Gramapurohit, Gosavi, & Phuge, ; Willaert et al, ). The species is sexually dimorphic with females being larger than males.…”